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Prosopagnosia with Topographical Difficulties 1 CORE Metadata, citation and similar papers at core.ac.uk Provided by Bournemouth University Research Online Prosopagnosia with topographical difficulties 1 Running Head: PROSOPAGNOSIA WITH TOPOGRAPHICAL DIFFICULTIES Developmental Prosopagnosia with Concurrent Topographical Difficulties: A Case Report and Virtual Reality Training Programme Sarah Bate, Amanda Adams, Rachel Bennetts & Hannah Line Department of Psychology, Bournemouth University, UK Word count: 6858 Address for correspondence: Dr Sarah Bate Department of Psychology Faculty of Science and Technology Poole House Bournemouth University Fern Barrow Poole BH12 5BB United Kingdom Telephone: +44 (0) 1202 961918 Fax: +44 (0) 1202 965314 Email: [email protected] Prosopagnosia with topographical difficulties 2 Abstract Several neuropsychological case studies report brain-damaged individuals with concurrent impairments in face recognition (i.e. prosopagnosia) and topographical orientation. Recently, individuals with a developmental form of topographical disorientation have also been described, and several case reports of individuals with developmental prosopagnosia provide anecdotal evidence of concurrent navigational difficulties. Clearly, the co-occurrence of these difficulties can exacerbate the negative psychosocial consequences associated with each condition. This paper presents the first detailed case report of an individual (FN) with developmental prosopagnosia alongside difficulties in topographical orientation. FN’s performance on an extensive navigational battery indicated that she primarily has difficulties in the formation and retrieval of cognitive maps. We then evaluated the effectiveness of a short-term virtual reality training programme and found that she is able to form a cognitive map of a particular environment following intense overlearning. Surprisingly, FN’s performance on a face recognition task also improved following training. While the latter finding was unexpected and requires further exploration, the training programme reported here may help to alleviate some of the compounded negative psychosocial consequences that are associated with difficulties in finding both locations and people. Keywords: Developmental prosopagnosia; topographical disorientation; navigation; cognitive map; face recognition. Prosopagnosia with topographical difficulties 3 Developmental Prosopagnosia with Concurrent Topographical Difficulties: A Case Report and Virtual Reality Training Programme 1. Introduction Prosopagnosia is a cognitive condition characterized by a relatively selective deficit in face recognition. While some individuals acquire the disorder following neurological injury or illness (e.g. Damasio, Damasio, & Van Hoesen, 1982; Bate et al., 2015), people with developmental prosopagnosia (DP) fail to develop normal face recognition skills (e.g. Bate, Haslam, Jansari, & Hodgson, 2009; Bate & Cook, 2012; Bennetts, Butcher, Lander, Udale & Bate, 2015; Duchaine & Nakayama, 2006; Jones & Tranel, 2001). DP is sometimes referred to as ‘congenital’ or ‘hereditary’ prosopagnosia (for a discussion of terminology see Bate & Tree, 2017) and has been attributed to a failure to develop the visual recognition mechanisms necessary for successful face recognition, despite intact low-level visual and intellectual functions. While acquired prosopagnosia (AP) is a rare condition, recent reports suggest that DP affects approximately two per cent of the population (Bowles et al., 2009; Bennetts, Murray, Boyce, & Bate, 2017) and in some cases may be genetic in origin (Duchaine, Germine, & Nakayama, 2007; Kennerknecht et al., 2006). While both AP and DP are characterised by the hallmark symptom of impaired face recognition skills, it is still widely debated whether they are parallel conditions. In part this is because the functional and structural profile of AP is relatively well known in comparison to DP. While more work has focused on theoretically important dissociations within the two conditions (e.g. between face and object recognition or the recognition of facial identity and expression: Bate & Bennetts, 2015; Duchaine & Nakayama, 2005; Fisher, Towler & Eimer, 2017; Humphreys, Avidan & Behrmann, 2007, Palermo et al., 2011), less work has attempted to identify whether the accompanying deficits that are typically associated with AP also hold Prosopagnosia with topographical difficulties 4 for DP. This is an important consideration from an assessment and rehabilitation perspective: if other difficulties are commonly associated with DP, it is important that these are assessed and targeted via appropriate intervention techniques. One common association with AP is topographical disorientation (the inability to orient and navigate in familiar and unfamiliar surroundings: Berthoz, 2001; Wang & Spelke, 2002), where many objective (Hécaen & Angelergues, 1962; Aguirre & D’Esposito, 1999; Landis, Cummings, Benson & Palmer, 1986) and anecdotal (Barton, Press, Keenan, & O’Connor, 2002; Bauer, 1984; Malone, Morris, Kay, & Levin, 1982; Takahashi, Kawamura, Hirayama, Shiota, & Isono, 1995; Schmidt, 2015) reports suggest a long-standing relationship. These difficulties can be underpinned by impaired landmark and/or scene recognition, or by difficulties in the representation of spatial relationships (Aguirre & D’Esposito, 1999; Arnold et al., 2013; De Renzi, 1982; Liu, Levy, Barton, & Iaria, 2011). Although little work has attempted to map these different types of topographical impairment onto particular anatomic or functional subtypes of AP, one recent study concluded that the condition is typically associated with impaired place recognition, together with poor cognitive map formation (mental representations of a person’s surrounding, including landmarks and the spatial relations between them: O’Keefe & Nadel, 1978) in cases of occipitotemporal damage (Corrow et al., 2016). Anecdotal evidence also indicates that topographical disorientation may be prevalent in DP (e.g. Brunsdon, Coltheart, Nickels, & Joy, 2006; Duchaine, Parker, & Nakayama, 2003; Jones & Tranel, 2001; Le Grand et al., 2006; McConachie, 1976), although only two reports to date have formally investigated this possibility. Klargaard, Starrfelt, Peterson and Gerlach (2016) found that four out of nine DPs performed significantly poorer than controls on a memory task that required the retention of topographic information. In the AP paper described above, Corrow and colleagues (2016) also assessed the navigational skills of seven Prosopagnosia with topographical difficulties 5 adults with DP. Contrary to the patterns of topographical disorientation observed in the AP participants, atypicalities only emerged on one task (cognitive map formation) in one DP participant, leading the authors to conclude that DP may be a more face-selective disorder than AP. While this certainly may be the case, it is notable that six of the seven DP participants (including the one that displayed atypical performance on the cognitive map test) did not self-report navigational difficulties in an initial interview. Thus, the frequency that topographical disorientation and DP co-occur may be under-represented in this study. Further, it has recently become clear that topographical disorientation can occur in developmental cases. For instance, Bianchini et al. (2010) described a 22 year-old man with severe developmental topographical disorientation (DTD) who was severely impaired at processing the spatial relationships between the parts of a whole stimulus; and Iaria and Barton (2010) reported 120 people with DTD who had an inability to form cognitive maps. Iaria, Bogod, Fox and Barton (2009) carried out a thorough cognitive and neural examination of a woman with DTD. Behavioural assessments in real-world and virtual reality environments also revealed an inability to form cognitive maps, with a corresponding lack of activation in the hippocampal complex and retrosplenial cortex – regions that were activated in control participants performing the same task. In sum, most reports of DTD to date indicate that the primary impairment in developmental cases may be the formation and retrieval of cognitive maps. However, it remains unclear whether this difficulty is absolute, or if it can at least to some extent be alleviated by over-rehearsal or training within a given environment. This is a pertinent issue for individuals who simultaneously experience DP and topographical difficulties, given the combined impact of these difficulties on socio-emotional functioning. Indeed, some reports suggest that DP can have detrimental effects on a person’s social and occupational interactions (e.g. Yardley, McDermott, Pisarski, Duchaine, & Prosopagnosia with topographical difficulties 6 Nakayama, 2008; Dalrymple et al., 2014), and it is conceivable that the stress and anxiety experienced in such situations would either be further exacerbated by poor navigational skills (e.g. when required to locate a meeting spot and then to subsequently identify a particular person within that location), or increase or bring about the disorientation difficulties themselves. While there have been some attempts to improve face recognition skills in DP (e.g. Bate et al., 2014; DeGutis, Bentin, Robertson, & D’Esposito, 2007; DeGutis, Cohan, & Nakayama, 2014), results are varied and no clear treatment strategy has yet emerged (Bate & Bennetts, 2014). Likewise, few attempts have been made to improve topographical difficulties (but see Brunsdon, Nickels, Coltheart, & Joy, 2007; Bouwmeester,
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